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Freshwater Snails of Biomedical Importance in the Niger River Valley

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Freshwater Snails of Biomedical Importance in the Niger River Valley Rabone et al. Parasites Vectors (2019) 12:498 https://doi.org/10.1186/s13071-019-3745-8 Parasites & Vectors RESEARCH Open Access Freshwater snails of biomedical importance in the Niger River Valley: evidence of temporal and spatial patterns in abundance, distribution and infection with Schistosoma spp. Muriel Rabone1* , Joris Hendrik Wiethase1, Fiona Allan1, Anouk Nathalie Gouvras1, Tom Pennance1,2, Amina Amadou Hamidou3, Bonnie Lee Webster1, Rabiou Labbo3,4, Aidan Mark Emery1, Amadou Djirmay Garba3,5 and David Rollinson1 Abstract Background: Sound knowledge of the abundance and distribution of intermediate host snails is key to understand- ing schistosomiasis transmission and to inform efective interventions in endemic areas. Methods: A longitudinal feld survey of freshwater snails of biomedical importance was undertaken in the Niger River Valley (NRV) between July 2011 and January 2016, targeting Bulinus spp. and Biomphalaria pfeiferi (intermedi- ate hosts of Schistosoma spp.), and Radix natalensis (intermediate host of Fasciola spp.). Monthly snail collections were carried out in 92 sites, near 20 localities endemic for S. haematobium. All bulinids and Bi. pfeiferi were inspected for infection with Schistosoma spp., and R. natalensis for infection with Fasciola spp. Results: Bulinus truncatus was the most abundant species found, followed by Bulinus forskalii, R. natalensis and Bi. pfeiferi. High abundance was associated with irrigation canals for all species with highest numbers of Bulinus spp. and R. natalensis. Seasonality in abundance was statistically signifcant in all species, with greater numbers associated with dry season months in the frst half of the year. Both B. truncatus and R. natalensis showed a negative association with some wet season months, particularly August. Prevalences of Schistosoma spp. within snails across the entire study were as follows: Bi. pfeiferi: 3.45% (79/2290); B. truncatus: 0.8% (342/42,500); and B. forskalii: 0.2% (24/11,989). No R. natalensis (n 2530) were infected. Seasonality of infection was evident for B. truncatus, with highest proportions shedding in the= middle of the dry season and lowest in the rainy season, and month being a signifcant predictor of infection. Bulinus spp. and Bi. pfeiferi showed a signifcant correlation of snail abundance with the number of snails shedding. In B. truncatus, both prevalence of Schistosoma spp. infection, and abundance of shedding snails were signifcantly higher in pond habitats than in irrigation canals. Conclusions: Evidence of seasonality in both overall snail abundance and infection with Schistosoma spp. in B. truncatus, the main intermediate host in the region, has signifcant implications for monitoring and interrupting trans- mission of Schistosoma spp. in the NRV. Monthly longitudinal surveys, representing intensive sampling efort have provided the resolution needed to ascertain both temporal and spatial trends in this study. These data can inform planning of interventions and treatment within the region. *Correspondence: [email protected] 1 Department of Life Sciences, Natural History Museum, Cromwell Rd, South Kensington, London SW7 5BD, UK Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Rabone et al. Parasites Vectors (2019) 12:498 Page 2 of 20 Keywords: Schistosomiasis, Freshwater snails, Seasonality, Niger, Bulinus, Biomphalaria, Schistosoma, B. truncatus, B. forskalii, B. pfeiferi, R. natalensis, S. haematobium, S. bovis, S. mansoni Background has impacted schistosomiasis distributions by alter- Schistosomiasis is a neglected tropical disease (NTD) ing available habitat for freshwater snail intermedi- afecting over 200 million people worldwide, with an at- ate hosts [23]. Some recent studies have shed light on risk population estimated at 700 million [1]. It is caused abundance and distribution of these snail species at by digenean trematodes of the genus Schistosoma. diferent spatial and temporal scales, both in the NRV Te complex indirect life-cycle involves an intermedi- and in sub-Saharan Africa as a whole [26–32]. How- ate freshwater snail host and transmission is through ever, substantial knowledge gaps remain. In addition, water contact. Te distribution of schistosomes directly there is often a mismatch between intermediate host relates to the geographical range of their intermedi- snail abundance and distribution and snail infection, let ate snail hosts. Tis is infuenced by factors including alone between snail infection levels and human schis- climate, altitude, rainfall, water chemistry and aquatic tosomiasis transmission [33–36]. For example, analysis vegetation [2]. Schistosomiasis is present through- of a recent outbreak of urogenital schistosomiasis in out West Africa, including Niger. Urogenital schisto- Corsica found evidence of ongoing transmission but no somiasis is endemic in the Niger River Valley (NRV), infected Bulinid snails [37]. It is not clear if this is due and is caused by Schistosoma haematobium, the most to insufcient sampling, the characteristic low levels widespread and prevalent human schistosome species of infection (and latent infection period) in snails, or if across Africa, which displays often severe patholo- transmission is so patchy that there is little correlation gies [3–6]. Schistosoma bovis, a pathogen of domestic of snail abundance and infection prevalence, and result- livestock and some non-domestic artiodactyls [7] is ing transmission [38]. Schistosomiasis is highly focal, also prevalent in the region [8–11]. Schistosoma hae- requiring overlap of intermediate and defnitive hosts matobium and S. bovis have overlapping distributions [24], and multiplication of the larval cercaria stage in across mainland Africa [12], and can infect several dif- snails can continue transmission even with very low ferent species of the freshwater snail genus Bulinus as snail infection prevalence [37]. Recent reviews there- their intermediate hosts [13–15]. Tese two species of fore highlight the crucial importance of snail surveys schistosome show evidence of hybridization in several to aid understanding of transmission, and to improve West African countries, including Niger, complicat- predictive modelling of future schistosomiasis distribu- ing disease control [16–20]. In addition, the NRV has tions in relation to climate change and schistosomiasis localised areas of intestinal schistosomiasis [21], which control [39–41]. Currently there is a focus on longitu- appear to be spreading (A. Garba, personal communi- dinal survey data across years, and critically, seasons, cation). Intestinal schistosomiasis is caused by Schis- to characterize snail populations with more precision tosoma mansoni, which infects over 83 million people [42]. Tese surveys require accurate identifcation of across sub-Saharan Africa, the Middle East, parts of snails and schistosome cercariae to provide high quality South America and some Caribbean islands [22, 23]; data to support treatment program activities and con- snail species of the genus Biomphalaria act as the inter- tribute to schistosomiasis knowledge more widely. Te mediate host [24]. Schistosomiasis Consortium for Operational Research Together, the multiple snail and schistosome species and Evaluation programme (SCORE, https ://score .uga. result in a complex and persistent pattern of schis- edu) has recently undertaken studies to investigate and tosomiasis transmission in Niger, infuenced by the quantify the factors related to snail-human infection country’s geography. Te Niger River, which crosses processes within the context of mass drug administra- approximately 550 km of western Niger, is the country’s tion strategies in fve African countries, including Niger main water supply, critical in a country which is two- [43]. Among other study goals, the programme aimed thirds desert [25]. Te catchment is home to freshwa- to address the gap in longitudinal abundance and dis- ter snail species of biomedical importance, including tribution data for intermediate freshwater snail hosts to the pulmonate snails Bulinus truncatus, B. globosus, help inform public health planning for schistosomiasis B. senegalensis, B. forskalii and Biomphalaria pfeiferi, control within Niger. Here, we report on longitudinal all acting as hosts for Schistosoma spp., and Radix surveys, carried out in the context of the SCORE stud- natalensis, a host for Fasciola spp. [24]. Studies have ies, for several species of freshwater snails of biomedi- been undertaken in West Africa on how dam building cal importance in the Niger River Valley. Specifcally, Rabone et al. Parasites Vectors (2019) 12:498 Page 3 of 20 this study conducted surveys to identify Schistosoma surveyed every month (apart from April in 2014 and spp. transmission sites and to determine the intermedi- 2015 due to logistical reasons). Site selection was based ate snail hosts (particularly Bulinus spp.) at these sites on
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